Organ blood flow and vessels of microcirculatory bed ... - Springer Link

ISSN 00220930, Journal of Evolutionary Biochemistry and Physiology, 2006, Vol. 42, No. 3, pp. 243—252. © Pleiades Publishing, Inc., 2006. Original Russian Text © A. A. Soldatov, 2006, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2006, Vol. 42, No. 3, pp. 193—200.

REVIEWS

Organ Blood Flow and Vessels of Microcirculatory Bed in Fish A. A. Soldatov Institute of Biology of Southern Seas, National Academy of Sciences of Ukraine, Sevastopol, Ukraine Received April 20, 2005

Abstract—Information on density of fish capillary network and its permeability, peculiarities of ge ometry, morphology, and ultrastructure of vessels of microcirculation bed—arterioles, venules, cap illaries—is presented. A great attention is paid to vasomotor reactions and their participation in re distribution of blood. Nervous and humoral mechanisms of control of tone of the vessel smooth muscle wall and voluminous blood flow are considered. Effects of environmental factors on pro cesses of microcirculation in fish are discussed. DOI: 10.1134/S002209300603001X

INTRODUCTION

DENSITY OF THE CAPILLARY NETWORK

Parameters of microcirculation produce an es sential effect on character of PO distribution in tis 2 sues. Geometry of vessels of capillary bed and their density determine area of diffusion surface and thickness of the diffusion layer. In the higher ver tebrates, reactions of blood flow redistribution are able to realize a fast correction of the tissue PO . 2 However, this ability has been reached in evolu tion not at once. Cyclostomata have a poorly de veloped system of microcirculation [1]. Cartilagi nous and bony fish represent the first groups of or ganisms whose density of the capillary network in tissue structures is close to that in terrestrial verte brates [2, 3]. However, in the structuralfunction al aspect, their vascular system has several princi pal peculiarities: differences in reactivity of vessels to vasoactive compounds and ecological factors [4–8], heterogeneity of vessels of the capillary bed [9–11], high permeability of capillary units to or ganic compounds [12, 13], presence of the second ary circulating system [14, 15], etc. The goal of the present work is to summarize this information.

Comparative studies have shown that the num ber of functioning capillary units and mitochon drial volume of skeletal muscles in fish are close to those in birds and mammals [2, 3]. However, the estimated indexes—capillary length vs. mitochon dria volume; capillary surface vs. mitochondria volume—were, on the contrary, much lower. This means that delivery of oxygen to mitochondria in fish is less efficient. One of peculiarities of fish skeletal muscles is spatial subdivision of the red and white muscle tis sues [16]. Special studies carried out on the flat head Platycephalus bassensis using an acrylic plas tic Мегсох has shown that red muscles are sup plied with five main branches of intermuscle ar teries, whereas white muscles—predominantly by spinal and abdominal segmentary arteries [17]. This means that these types of muscles have their own systems of blood supply, the capillary network density differing essentially in the red and white muscle tissues. It is much higher in the former, which correlates directly with the number of mi

243

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tochondria in muscle fibers. This fact has been re ported in works of many authors [18, 19]. Thus, in the cartilaginous fish red muscles the capillaries cover 18–25% of the muscle fiber surface, while in the white ones—0.2–9.0% [20]. Similar data have also been obtained in bony fish [21]. In cy clostomes (river lamprey), white muscles were not vascularized at all, while in the red ones the capil lary net is located only on their surface [1]. Regular differences in the number of function ing capillary units in muscle tissue have also been detected in two ecological fish groups differing by the level of natural motility—benthic and pelagic. In the latter the capillary network density in both types of muscles was much higher [22, 23]. The most pronounced differences were found in the red muscle tissue. In mobile species (Baikal cisco, grayling), in red and white muscles there were 760– 870 and 90–95 capillaries, respectively, per 1 mm2 of crosssection, whereas in the lowactive fish (perch, ide, goldfish) these values amounted to 560–680 and 80–90 capillaries, respectively [21]. Several peculiarities in vascularization of the muscle tissue have also been established in repre sentatives of the Antarctic fish fauna. Their mus cle tissue had a close or the larger mitochondrial volume in comparison with fish of middle latitudes, the capillary network density being essentially low er [24, 25]. Such peculiarities of vascularization correlated with changes of geometry of function ing capillaries, as this will be discussed below. It is also to be noted that in the Antarctic fish the num ber of capillary units in white and red muscles was close [23]. The experimental hypothermia did not produce similar changes in skeletal muscles of fish of middle latitudes. Thus, the superficial and vo luminous density of capillaries in muscle tissue of the European eel at 10 and 29°C coincided abso lutely [26]. Regular changes in parameters of tissue capil larization are also noted in fish of hypoxic aquato ria, constantly dealing with oxygen deficit. The capillary network density rose in structures the most sensitive to PO (brain, heart) [27], the num 2 ber of functioning capillary units in skeletal mus cles practically being not changed [28]. One of peculiarities of the capillary network of fish tissues is the presence of the secondary circu latory system. It is formed at the level of interarte

rial anastomoses, from which the secondary cap illaries and then venules run [14]. The blood flow ing through this capillary network contains the negligible number of erythrocytes, i.e., its partici pation in oxygen supply of tissues is less essential, than of capillaries of the primary circulating sys tem. It is noted that the secondary capillary units resemble by their structure the mammalian lym phatic capillaries [15]. Therefore, this group of ves sels is assumed to be a component of the fish lym phatic system. GEOMETRY, MORPHOLOGY, AND ULTRASTRUCTURE OF MICROCIRCULATION VESSELS Capillaries. Linear sizes of functioning capillary units in fish skeletal muscles have apparently ex pressed tissue specificity. There is practically in verse correlation between the tissue capillary net work and geometrical parameters of individual ves sels. In red muscles, capillaries, with their higher density, are shorter and thinner (diameter of 9– 13, length of 470–770 µm), whereas in white mus cles, on the contrary, they are longer and wider (diameter of 50–73, length of 890–1300 µm). This regularity has been established in many freshwater and marine fish species [21, 23, 26]. It is also con firmed by vital microscopy methods [29]. In Antarctic fish, the pattern somewhat differs. They have rarely distributed large vessels, whose linear sizes (64 ± 7 µm in diameter) correspond to those of white muscle capillaries of the majority of fish [24]. Tissue specificity is not expressed [23]. In opinion of the authors, such organization of the capillary bed promotes intensive blood flow in tis sue and is aimed at maintaining a high blood–pa renchyma gradient of PO , which promotes diffu 2 sion processes. Capillary walls are formed by endothelial cells whose thickness is 0.04–0.05 µm in bony fish and 0.10–0.50 µm in cyclostomes [30, 31]. Their cy toplasm is poorly developed and practically does not contain organelles [30]. Cells are closely adja cent to each other densely; however, locally there are ruptures and holes, about 60 nm in diameter. The number of the holes is higher in the venous, than in arterial part of the capillary [9, 10]. Des mosomes, whose structure can include smooth

JOURNAL OF EVOLUTIONARY BIOCHEMISTRY AND PHYSIOLOGY Vol. 42 No. 3 2006

ORGAN BLOOD FLOW AND VESSELS OF MICROCIRCULATORY BED IN FISH

reticulum, are often revealed between the endot helial cells [31]. In the fish capillary endothelium, sufficiently frequently there are present vacuole like structures interacting actively with extracellu lar cavities [32]. Thickness of the fish blood–parenchyma barri er amounts to about 0.188 µm [30]. The arterial extremity of the capillary is usually thicker, which is due to the better development of endothelium [9]. Apart from the endothelial layer, capillary wall can contain pericytes and the basal membrane [30, 33]. The basal membrane is not characteristic of capillaries of cartilaginous fish [34]. Organization of pericapillary space also affects thickness of the blood–parenchyma barrier in fish. Thus, in cyclos tomes, a high content of proteoglycans, glycopro teins, tubulin microfibrils, and collagen fibers is found in this zone [31]. The above differences in structure of arterial and venous ends of the capillary seem to be due to pe culiarities of their formation. The fish capillaries have been shown to develop either from single cells with a large vacuole or as a result of cytoplasmic contact of one or several cells to connective tissue complex [35]. Formation of capillaries of two types is possible: of the venous and arterial ones that dif fer by the endothelium structure and permeability [11]. To specify details of formation of capillary structures in fish, a procedure of cultivation of their cells is developed [36]. Comparative studies of permeability of capillar ies in mammals and fish have shown it to be al most 10 times higher in the latter [12]. It has turned out that the fish capillary network is highly perme able for proteins [37]. This was indicated by close concentrations of protein compounds in capillary and extracapillary spaces. Special studies carried out on river eel have confirmed this suggestion with respect of albumin [13]. It is also found that per meability of capillaries to this group of proteins, sucrose, Na+, and water depends on temperature. No such dependence on oxygen is revealed. Functioning of the capillary network is substan tially determined by the state of the adjacent ves sels (arterioles and venules). Arterioles and venules. Electron microscopy stud ies have shown the ultrastructure of arterioles in fish to be close to that in mammals [34]. Arterioles usually have one layer of smooth muscle elements

245

and contain the basal membrane [9, 38]. At the same time, there also are several peculiarities. Thus, in endothelial cells of Parica scuber [38], microfilaments located along vessels are detected, while on the internal surface of arterioles of Ce prinodon variegates—specific periendothelial cells with high content of actinlike fibers [33]. Func tional significance of these elements of structure is not yet clear. An important point in study of mi crocirculation bed of fish vessels was detection of sphincters in precapillary arterioles of trout spleen [39]. This means that the blood flow in this organ can be controlled by changes not only of tone of the smooth muscle wall, but also of the number of functioning capillary units. In venules of fish, unlike mammals, the smooth muscle layer appear not at once, but only in ves sels of the 300µm diameter, whereas in mammals this occurs already in venules of the 50µm diame ter [34]. The presence of the basal membrane in the venule wall structure is determined not as un ambiguously as in arterioles. It is not pronounced in cartilaginous fish (dogfish) [34], whereas is well developed in bony fish Регса fluviatilis and Misqur nus fossilis [9]. Periendothelial cells with a high content of actinlike fibers have been found in ve nules of Ceprinodon variegatus as well as in its arte rioles [33]. VASOMOTOR REACTIONS As shown by observations, reactions of blood redistribution take a sufficiently active part in ad aptation of the fish organism to environmental conditions. The most expressed effect was pro duced by external hypoxia. However, its action on vessels was ambiguous. In most cases, vasodilator effect was observed. Similar reactions have been detected in vessels of gill lamellas [40], brain [41, 42], coronary vessels [6]. The number of function ing capillary units was simultaneously elevated. This was indicated by an increase of the amount of perfused branchial lamellas in trout under condi tions of oxygen deficiency [43]. But in experiments by Ristori and Laurent [44] the opposite data were obtained. Arterial vessels of trout gills under con ditions of experimental hypoxia were submitted to pronounced vasoconstriction, while reaction of venous bed vessels was not obvious. It was also no


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ticed that pressor effect of hypoxia occurred with rising of KCl concentration in the medium. This allows suggesting participation of K+channels in action of low PO values on the tone of the smooth 2 muscle vessels wall [45]. Vasodilator effect on fish vessels by NO [46] and low temperatures [40] was detected. Regular redis tribution of systemic blood flow was also observed in fish under conditions of experimental floating [47] and of action of acid medium [48]. All the above indicates that the fish organism has rather efficient mechanisms of correction of tone of the smooth muscle blood vessel wall. The state of the fish vascular wall is controlled by nervous and humoral pathways. The role of ner vous regulation has been shown to increase in the series cyclostomes—osteocartilaginous—cartilag inous—bony fish [49]. Cholinergic vasodilator ef fects on fish vessels are noted [50, 51]. Using fluo rescent labels, the presence of sympathetic nerve ending was also shown convincingly in large arter ies, arterioles of digestive tract, and venous sinus of 6 marine fish species [52]. It has been found that the sympathetic innervation promoting constric tion of arteriovenous pathways is realized through αadrenoreceptors [53], while dilation—through βadrenoreceptors [51]. The data obtained both in vivo and in vitro indi cate the existence of α and βadrenoreceptors in the fish vascular wall [50, 51]. It has been shown that adrenaline and compounds structurally close to it (noradrenaline, isoprenaline) can produce both pressor and depressor effect on fish vessels [4, 43, 47, 54, 55]. Differences are the most expressed with respect to the vascular system of heart [5, 51, 56] and intestinal tract [57], the pressor reaction being eliminated by phentolamine (αadrenergic blocker), while the depressor one—by propranolol (βadrenergic blocker) [58, 59]. Use of 3Нadren aline and 3Нnoradrenaline has allowed establish ing areas of the densest accumulations of α and βadrenoreceptors in the fish vascular system [60]. As shown by observation, incorporation of these compounds occurred mainly in the region of the cardinal vein (chromaffin tissue), pronephros, kid ney, heart, and branchial filaments. Similar results have been obtained using immunochemical meth ods [51]. Expressed vasopressor action on fish vessels was

produced by acetylcholine. This reaction has been reported mainly in vessels of gills [43] as well as of brain [46] and heart bulb wall [51]. The effect of acetylcholine was abolished by atropine [58]. This proves the presence of cholinergic receptors in the fish vascular wall. Also observed was the pressor effect of serotonin. A comparatively higher con centration of this compound was revealed in gills of various systematic groups of marine fish [48, 61]. Administration of methysergide blocked 5HT receptors and abolished serotonin action [61], which indicates selective sensitivity of the vascular wall to this compound. Recently a particular attention has been paid to the fish renin–angiotensin system. The pressor ef fect of angiotensin II in mammals is commonly known. However, in fish, this compound not al ways produces the unambiguous action. The marked pressor effect has been described only in Pagothenia borchgrevinki [47]. In the American eel, more efficient was angiotensin III. The authors associate this with the presence of Сterminal Phe8 [62]. In the longhorn sculpin Myoxocephalus octo decinispinsus, the vascular system was not sensitive at all to this group of compounds [63]. Similar data were also obtained in cartilaginous fish [63]. The lack of the angiotensin II effect on the vascular sys tem of this systematic group of fishes seems to be due to the presence in their blood of a specific group of kinins: scyliorhinins I and II. Introduc tion of these compounds into the systemic blood flow of bony fish (trout) also produced response reactions of their vascular system [64]. This allows suggesting that the renin–angiotensin system in fish has pronounced molecular specificity. Adenosine and structurally close N6cyclopen tyladenosine are accepted as sufficiently potent vas oconstrictors in fish. They have been shown to pro duce the unambiguous pressor effect on the major ity of vessels of arterial and venous beds [44, 65]. Injection of aminophylline and 8cyclopentyltheo phylline abolishes this action [41, 65], which indi cates the presence of adenosine receptors in the vas cular wall. At the same time, the data also are ob tained on the depressor action of this compound. A similar reaction is detected in the cardinal vein in trout and some Antarctic fish [45, 65]. This allows suggesting the existence of at least two groups of adenosine receptors in the vascular wall.



247

Voluminous rate of blood flow in tissues of marine and freshwater fish Tissue

Blood flow (ml min–1 kg–1)

Method of registration

Reference

Australian eel

ventral aorta

11.4

thermistor sensors

[79]

Anguilla rostrata

dorsal aorta

29.5

labeled microspheres

[62]

Salmo gairdneri

hepatic vein

12.5

doppler telemetry

[77]

white muscles

0.2–0.4


[72]

red muscles

0.7–3.5

the same

[72]

white muscles

0.7–1.1

H2clearance

[80]

red muscles

1.9

the same

[80]

Hemilepidotus hemilpidotus

abdominal artery

4.1 ± 0.6


[57]

The same

mesenteric artery

4.9 ± 1.3

the same

[57]

Galeorhinus australis

heart

0.28

the same

[81]

Salmo gairdneri

heart

0.14

"

[56]

Fish species

Thymallus arcticus The same Thymallus arcticus baicalensis The same

An expressed pressor action of arginine–vaso tocin and isotocin also has been revealed. Howev er, the authors observed that this reaction had de veloped only at the much higher compound con centrations certainly exceeding the physiological norm [66, 67]. Phentolamine [68] and atriopeptin [69] belong to compounds of the depressor type and are effi cient with respect to the smooth muscle wall of fish vessels. It is noticed that atriopeptin is produced by cardiac ventricle and produces a predominant action on gill vessels. According to its immunoche mical properties, it is close to human atriopeptin. Also revealed is the expressed vasodilator effect of NO on brain vessels. Its content increases under hypoxic conditions [46] and is associated with an increased activity of NOsynthase in brain tissue [42]. With respect to hypercapnia, such depen dence is not found [8]. Alongside with systemic mechanisms of correc tion of tone of smooth muscle vascular wall, sev eral local vasoactive factors also are found in fish. They include, first of all, pH value. Under condi tions in vitro, acidification has been shown to pro duce depressor effect on branchial, intestinal, me senteric arteries and cardiac vein of trout, while alkalization causes the opposite action [45]. A sim ilar effect of pH value is also revealed on gill ves

sels under conditions of their experimental perfu sion [45]. Recently, in skeletal muscles of Centro pristis striata, there has been immunochemically identified prokallikrein (36 kDa) that acquired bi ological active (depressor effect) in the dimer state (72 kDa) [70]. This substance at a somewhat lower concentration was revealed in heart, spleen, kid neys, gills, and swim bladder [70]. Later, prokal likrein has also been found in tissues of other fish [71]. A group of various intestinal neuropeptides also is to ascribe to substances producing the local vasoactive effect [49]. VOLUMINOUS TISSUES BLOOD FLOW Control of voluminous blood flow in tissues of fish presents certain methodical difficulties. Anal ysis of publications has shown a sufficiently exten sive methodical arsenal used by researchers. The most widely spread is the method with use of dex trin microspheres of about 15 µm diameter of par ticles impregnated with 85Sr or 51Cr [62, 72–76]. It allows estimating not only the rate, but also dis tribution of the blood flow. Especially popular is the Doppler laser flowmeter [47, 65, 77, 78]. Ther mistor sensors implanted into vessels [79] and the method of Н2clearance with an electrochemical generation of hydrogen [21, 80] are of limited use.


248

SOLDATOV

In experiments on the catfish Hypostomus puncta tus an attempt was made to record the linear blood flow. Measurements were performed on thoracic fins using vital microscopy and video shooting [29]. The results obtained using the above methods are presented in the table; as seen from the table, the values obtained by different methods have turned out to be close. This means that the methodical specificity of the obtained data actually is not pro nounced. As expected, the highest rates of the vo luminous blood flow are found in the large vessels (dorsal and ventral aortas, hepatic portal vein)— 11–18 ml min–1 kg–1. Study of the blood flow dis tribution in the catfish Ictalurus punctatus by the method of radioactive microspheres has shown that 72% of the heart output are in white muscles, 5.7%—in head kidney, 5.5%—in red muscles, 3.1%—in stem kidneys, 2.2%—in liver, 1.4%—in swim bladder, 1.1%—in skin, and less than 0.5%— in stomach, intestine, gonads, brain, spleen, and other organs [76]. The authors have noted that the blood flow in muscles is not uniform. Similar data have been obtained in the tuna Thunnus alalunga and the Arctic grayling Thymallus arcticus [72, 75]. The observations have shown that environmen tal factors and the state of individuals produce an essential effect on the value of the fish voluminous blood flow. Significant redistribution of blood oc curred under conditions of external hypoxia. Ce rebral and coronary blood flows increased more than twice [6–8, 41, 56]. Meanwhile in kidneys, liver, spleen, and skeletal muscles the blood flow was preserved at the initial level [72], whereas in intestinal arteries it was markedly reduced [68]. Changes of the fish blood flow also occur at a change of environmental temperature. In the coast trout an elevation of temperature in the range of 6–18°C produced an activation of blood flow in white muscles and its decrease in spleen, liver, kid neys, intestine, and gallbladder [74]. An increase of the cerebral blood flow is detected in carp [82]. In other organs and red muscles, it did not change. The blood distribution pattern was also affected by changes of environmental salinity. With its rise, a marked increase of cutaneous blood flow was re vealed in Pleuronectes platessa [83]. Quite a few works study the fish blood flow un der conditions of physical activity. When swim ming in a cruising regime, a regular redistribution

of pressure occurred between the dorsal and ven tral aortas. It decreased in the dorsal aorta and in creased in the ventral one [47, 79]. A simultaneous rise of the blood flow by 60% was recorded in car diac muscle [73]. This rise was even more pro nounced in the white and red muscles [21, 73, 80, 84]. In other organs (liver, spleen, gastrointestinal tract) the blood flow, on the contrary, decreased [68]. At maximal speeds of swimming, further aug mentation of the voluminous flow rate of the blood circulation was revealed only in red muscles [21, 80]. In white muscles the blood flow was enhanced only after cessation of the loading [21, 73, 80]. The blood flow in an organ depends on qualita tive composition of vasoactive compounds in blood plasma and on sensitive to them of vascular wall receptors. Fish are not exception in this aspect. Sensitivity of individual parts of their cardiovas cular system to substances of the pressor and de pressor action is different. For example, the blood flow in gills was enhanced by atriopeptin and in hibited by adenosine [69]. At the same time, ade nosine activates the cerebral blood flow [41]. A si milar effect has also been found for acetylcholine [46]. The cardinal blood flow correlated positively with blood adrenaline level [5, 6]. However, this hormone produced a rather ambiguous effect on the spleen blood flow [4], etc. The data presented in this section of the review allows concluding that processes of microcircula tion in fish have several principal peculiarities. (1) Fish have the capillary network density in tis sues comparable with that in mammals and geom etry of capillary units close to them. This is suffi ciently unexpected considering a low intensity of metabolic processes in cells of poikilothermal an imals to which this taxonomic group of organisms belongs. (2) A characteristic peculiarity of the fish micro circulation is the presence of the secondary circu latory system that starts from arteriovenous anas tomoses. Its vessels practically do not contain blood cells; therefore their participation in oxygen sup ply of tissues has to be insignificant. (3) The capillary bed in fish is not uniform. There are several differences in structure and permeabil ity of the arterial and venous ends of the capillary, as well as between capillary units of the primary and secondary circulatory systems.



(4) The permeability of capillaries in fish is al most 10 times higher than in mammals. The pres ence of large holes and ruptures at the venous end of the capillary allows many highmolecular com pounds, proteins in particular, to permeate easily the blood–parenchyma barrier. (5) The most reactive sites of the fish circulatory system are vessels of brain, heart, gills, and kidneys. They are sensitive to many vasoactive compounds produced both by nerve endings and by endocrine glands. The reactions of blood flow redistribution in these organs are revealed in response to changes of temperature, oxygen content, and other situa tions. Vessels of skeletal muscles and other organs, on the contrary, poorly react to incoming actions. Significant changes of the blood flow are found only at periods of muscular activity. In other cas es, the vasomotor reactions are expressed weakly.

8.

9.

10.

11.

12.

13.

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